Speciation driven by ancestrally polymorphic chromosomal inversions

Chromosomal inversions may play a central role in speciation through their ability to reduce recombination and therefore genetic exchange at inverted parts of the genome between diverging populations. We analysed long- and short-read whole-genome data from sympatric and allopatric populations of two Drosophila virilis group species, D. montana and D. flavomontana, to understand how inversions have contributed to the divergence of these sister species. Using highly contiguous genome assemblies for both species, we identified three large alternatively fixed inversions on the X chromosome and one in each of the autosomes 2L, 4 and 5. A comparison of demographic models estimated for inverted and non-inverted (colinear) chromosomal regions suggest that these inversions most likely arose before or around the time of the species split. We also detected low rate of interspecific gene flow (introgression) from D. montana to D. flavomontana, which was further reduced inside inversions and was lower in allopatric than in sympatric populations. Together these findings suggest that the inversions have reduced gene exchange between these sister taxa both before and after the onset of species divergence and that low levels of recent introgression may have led to the reinforcement of reproductive barriers previously detected between these species. Our results suggest that ancestrally polymorphic inversions may act as drivers of speciation by allowing the accumulation of divergence inside inversions, while gene flow at colinear regions continues until the evolving reproductive barriers complete speciation.